Swarming motility in undomesticated Bacillus subtilis

Swarming motility was identified and characterized in an undomesticated strain of Bacillus subtilis. Rapid surface migration was preceded by a cell density‐dependent lag period, which could be eliminated if actively swarming cells were used as the inoculum. The leading edge of the swarm was characterized by multicellular rafts of highly flagellated cells. Flagellum biosynthesis and surfactant production were required for swarming. Swarming was not found in any of several standard laboratory strains. Laboratory strains are characteristically unable to produce surfactant, but such a strain remained unable to swarm even when surfactant was provided by extracellular complementation. We conclude that robust swarming is a feature of undomesticated B. subtilis and that this behaviour has been lost or attenuated in laboratory strains through the accumulation of multiple genetic defects.

[1]  C. Penn,et al.  Selection from gonococci grown in vitro of a colony type with some virulence properties of organisms adapted in vivo. , 1977, Journal of general microbiology.

[2]  E. Ghelardi,et al.  Swarming motility in Bacillus cereus and characterization of a fliY mutant impaired in swarm cell differentiation. , 2002, Microbiology.

[3]  G. Ordal,et al.  Activation of the CheA kinase by asparagine in Bacillus subtilis chemotaxis. , 1997, Microbiology.

[4]  F. Austin,et al.  Derivation of Extracellular Polysaccharide-Deficient Variants from a Serotype A Strain of Pasteurella multocida , 1999, Current Microbiology.

[5]  A. Grossman,et al.  Biochemical and genetic characterization of a competence pheromone from B. subtilis , 1994, Cell.

[6]  W. E. Inniss,et al.  A rapid, simple method for staining bacterial flagella. , 1977, Canadian journal of microbiology.

[7]  P. Stragier,et al.  Antibiotic-resistance cassettes for Bacillus subtilis. , 1995, Gene.

[8]  G. Macfarlane,et al.  Toxin Synthesis and Mucin Breakdown Are Related to Swarming Phenomenon in Clostridium septicum , 2001, Infection and Immunity.

[9]  R. Bourret,et al.  Purification and characterization of Bacillus subtilis CheY. , 1993, Biochemistry.

[10]  A. Goffeau,et al.  The complete genome sequence of the Gram-positive bacterium Bacillus subtilis , 1997, Nature.

[11]  E. Ghelardi,et al.  Requirement of flhA for Swarming Differentiation, Flagellin Export, and Secretion of Virulence-Associated Proteins in Bacillus thuringiensis , 2002, Journal of bacteriology.

[12]  R. Losick,et al.  Fruiting body formation by Bacillus subtilis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[13]  E. Moxon,et al.  The type b capsular polysaccharide as a virulence determinant of Haemophilus influenzae: studies using clinical isolates and laboratory transformants. , 1981, The Journal of infectious diseases.

[14]  G. Fraser,et al.  Swarming motility. , 1999, Current opinion in microbiology.

[15]  F. Young,et al.  Transduction in Bacillus subtilis by Bacteriophage SPP1 , 1974, Journal of virology.

[16]  M. Homma,et al.  The sodium‐driven polar flagellar motor of marine Vibrio as the mechanosensor that regulates lateral flagellar expression , 1996, Molecular microbiology.

[17]  J. Spizizen,et al.  TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. , 1958, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Chamberlin,et al.  The Bacillus subtilis flagellin gene (hag) is transcribed by the sigma 28 form of RNA polymerase , 1989, Journal of bacteriology.

[19]  R. Harshey,et al.  Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar function , 1992, Journal of bacteriology.

[20]  R. Harshey,et al.  The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  J. Adler.  Chemotaxis in Bacteria , 1966, Science.

[22]  G. Ordal,et al.  Cloning and characterization of genes encoding methyl-accepting chemotaxis proteins in Bacillus subtilis. , 1994, The Journal of biological chemistry.

[23]  R. Lenski,et al.  Loss of social behaviors by myxococcus xanthus during evolution in an unstructured habitat. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  H. Saxild,et al.  Functional and genetic characterization of mcpC, which encodes a third methyl-accepting chemotaxis protein in Bacillus subtilis. , 1997, Microbiology.

[25]  D. Sinderen,et al.  Sequence and analysis of the genetic locus responsible for surfactin synthesis in Bacillus subtilis , 1993, Molecular microbiology.

[26]  Joseph Watkins,et al.  Organized Cell Swimming Motions in Bacillus subtilis Colonies: Patterns of Short-Lived Whirls and Jets , 1999, Journal of bacteriology.

[27]  J. Helmann,et al.  Dual chemotaxis signaling pathways in Bacillus subtilis: a sigma D-dependent gene encodes a novel protein with both CheW and CheY homologous domains , 1994, Journal of bacteriology.

[28]  H. J. Conn.  The Identity of Bacillus Scbtilis , 1930 .

[29]  N H Mendelson,et al.  Patterns of reporter gene expression in the phase diagram of Bacillus subtilis colony forms , 1996, Journal of bacteriology.

[30]  J. Kirby,et al.  Chemotactic methylesterase promotes adaptation to high concentrations of attractant in Bacillus subtilis. , 1993, The Journal of biological chemistry.

[31]  M. Dixit,et al.  epr Is Transcribed from a ςD Promoter and Is Involved in Swarming of Bacillus subtilis , 2002 .

[32]  J. Kirby,et al.  CheC is related to the family of flagellar switch proteins and acts independently from CheD to control chemotaxis in Bacillus subtilis , 2001, Molecular microbiology.

[33]  A. Wach.  PCR‐synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cerevisiae , 1996, Yeast.

[34]  J. Kirby,et al.  Methanol production during chemotaxis to amino acids in Bacillus subtilis , 1997, Molecular microbiology.

[35]  M. Chamberlin,et al.  Sequence and characterization of Bacillus subtilis CheW. , 1992, The Journal of biological chemistry.

[36]  C. van Delden,et al.  Swarming of Pseudomonas aeruginosa Is Dependent on Cell-to-Cell Signaling and Requires Flagella and Pili , 2000, Journal of bacteriology.

[37]  G. Fraser,et al.  A motile but non‐swarming mutant of Proteus mirabilis lacks FlgN, a facilitator of flagella filament assembly , 1997, Molecular microbiology.

[38]  S. Molin,et al.  N-Acyl-L-homoserine lactone autoinducers control production of an extracellular lipopeptide biosurfactant required for swarming motility of Serratia liquefaciens MG1. , 1998, Journal of bacteriology.

[39]  M. Silverman,et al.  Flagellar dynamometer controls swarmer cell differentiation of V. parahaemolyticus , 1988, Cell.

[40]  R. B. Morrison,et al.  Swarming of Proteus—A Solution to an Old Problem? , 1966, Nature.

[41]  M. Nakano,et al.  Isolation and characterization of sfp: a gene that functions in the production of the lipopeptide biosurfactant, surfactin, in Bacillus subtilis , 1992, Molecular and General Genetics MGG.

[42]  P. Burkholder,et al.  Induced biochemical mutations in Bacillus subtilis. , 1947, American journal of botany.

[43]  R. Harshey,et al.  Differentiation of Serratia marcescens 274 into swimmer and swarmer cells , 1990, Journal of bacteriology.